Keywords
holothuroidea
marine protected area
reproductive season
sexual maturity
size structure
equinodermo
holothuroidea
área marina protegida
época reproductiva
madurez sexual
estructura de tamaño
How to Cite
Abstract
The population and reproductive biology of the commercial sea cucumber Holothuria mexicana (Ludwig, 1875) was studied in Southern Belize (Caribbean Sea), including the sex ratio, size at sexual maturity and reproductive cycle, as well as the size structure among habitats located inside and outside protected areas. Individuals found inside marine protected areas were consistently larger than individuals found outside these boundaries. The male:female sex ratio was 1.1:1.0 with a unimodal size distribution composed mainly of sexually mature individuals (87 %). Size at sexual maturity was established to be ~10 cm based on measures of gamogenetically mature individuals during the peak of the gametogenic maturity period. Juveniles and small adults measuring ≤ 15 cm (13 %), were collected exclusively in sandy and muddy areas of seagrass habitats associated with mangroves. Larger adults were commonly found on hard substrates in both seagrass-associated and coral-reef-associated habitats. Based on histology and gonad indices, the first sign of early gametogenesis was detected in August in both sexes. Gametes developed and matured throughout the colder months between November and February. Decreases in gonad index in both years suggest annual spawning, starting in March-April 2014 (single major event) and March-April and July-August 2015 (two smaller events) for both males and females. The spawning periods were correlated with warmer or increasing temperatures, low rainfall and increasing or high chlorophyll-a concentrations. These data will hopefully guide management and protection of the natural populations of H. mexicana, which are already suffering from overfishing in Belize and neighboring countries.
References
Abdel-Razek, F., Abdel-Rahman, S., El Shimy, N. A., & Omar, H. (2005). Reproductive biology of the tropical sea cucumber Holothria atra in the Red Sea coast of Egypt. Egyptian Journal of Aquatic Research, 31(2), 383-402.
Alvarado, J. J., Solis-Marin, F. A., & Ahearn, C. (2008). Equinoderms (Echinodermata) of the Central American Caribbean. Revista de Biologia Tropical, 56(Suplement 3), 37-55.
Amesbury, S. S., Callaghan, P., Hopper, D., Kerr, A., Martinez, P., & Richmond, R. H. (1996). Management of beche-de-mer resources in Micronesia. In R. H. Richmond (Ed.), Suggestions for the Management of Sea Cucumber Resources in Micronesia (pp. 32-41). Mangilao, Guam: University of Guam Marine Laboratory.
Anderson, S. C., Flemming, J. M., Watson, R., & Lotze, H. K. (2011). Serial exploitation of global sea cucumber fisheries. Fish and Fisheries, 12(3), 317-339.
Bakus, G. J. (1973). The biology and ecology of tropical holothurians. In O. A. Jones, & R. Endean (Eds.), Biology and geology of coral reefs (Vol. 11, Biology I, pp. 325-367). New York: Academic Press.
Balogh, R., Wolfe, K., & Byrne, M. (2018). Gonad development and spawning of the vulnerable commercial sea cucumber, Stichopus herrmanni, in the southern Great Barrier Reef. Journal of the Marine Biological Association of the United Kingdom (in press).
Belize Fisheries Department. (2013). South Water Caye. Retrieved from http://www.fisheries.gov.bz/south-water-caye
Birkeland, C., & Dayton, P. K. (2005). The importance in fishery management of leaving the big ones. Trends in Ecology and Evolution, 20, 356-358.
Bolaños, N., Bourg, A., Gómez, J., & Alvarado, J. J. (2005). Equinoderm diversity and abundance in the lagoon reefs in the Cahuita National Park, Caribbean Costa Rica. Revista de Biologia Tropical, 53, 285-290.
Bruckner, A. (Ed.). (2006). Proceedings of the CITES workshop on the conservation of sea cucumbers in the families Holothuriidae and Stichopodidae. Kuala Lampur, Malaysia. U.S. Department of Commerce, National Oceanic and Atmospheric Administration.
Bruckner, A. W., Johnson, K. A., & Field, J. D. (2003). Conservation strategies for sea cucumbers: Can a CITES Appendix II listing promote sustainable international trade? SPC Beche-de-Mer Information Bulletin, 18, 24-33.
Cameron, J. L., & Fankboner, P. V. (1986). Reproductive biology of the commercial sea cucumber Parastichopus californicus (Echinodermata: Holothuroidea). I. Reproductive periodicity and spawning behavior. Canadian Journal of Zoology, 64, 168-175.
Chao, S., Chen, C. P., & Alexander, P. S. (1994). Reproduction and growth of Holothuria atra (Echinodermata: Holothuroides) at two contrasting sites in southern Taiwan. Marine Biology, 119, 565-570.
Chao, S. M., Chen, C. P., & Alexander, P. (1995). Reproductive cycles of tropical sea cucumbers (Echinodermata: Holothuroidea) in southern Taiwan. Marine Biology, 122(2), 289-295.
Choe, S. (1963). Biology of the Japanese common sea cucumber Stichopus japonicus Selenka (Doctoral dissertation). Pusan National University, South Korea.
Conand, C. (1981). Sexual cycle of three commercially important Holothurian species (Echinodermata) from the lagoon of New Caledonia. Bulletin of Marine Science, 31(3), 523-543.
Conand, C. (1982). Reproductive cycle and biometric relations in a population of Actinopyga echinites (Echinodermata: Holothuroidea) from the lagoon of New Caledonia, western tropical pacific. In J. M. Lawrence (Ed.), International Echinoderm Conference (pp. 437-442). Tampa Bay, Florida, USA: Balkema, Rotterdam.
Conand, C. (1993a). Reproductive biology of the holothurians from the major communities of the New Caledonian Lagoon. Marine Biology, 116, 439-450.
Conand, C. (1993b). Ecology and reproductive biology of Stichopus variegatus an Indo-Pacific coral reef sea cucumber (Echinodermata: Holothuroidea). Bulletin of Marine Science, 52(3), 970-981.
Conand, C. (2006). Sea cucumber biology, taxonomy, distribution: conversation Status. In A. W. Bruckner (Ed.), Proceeding of the technical workshop on the conservation of sea cucumbers in the families Holothuridae and Stichopodidae (pp. 35-50). Kuala Lumpur, Malaysia: NOAA Technical Memorandum.
Conand, C., Uthicke, S., & Hoareau, T. (2002). Sexual and asexual reproduction of the holothurian Stichopus chloronotus (Echinodermata): a comparison between La Reunion (Indian Ocean) and east Australia (Pacific Ocean). Invertebrate Reproduction & Development, 41(1-3), 235-242.
Costelloe, J. (1985). The annual reproductive cycle of the holothurian Aslia lefevrei (Dendrochirota: Echinodermata). Marine Biology, 88(2), 155-165.
Desurmont, A. (1996). Spawning and asexual reproduction of tropical holothurians. SPC Beche-de-mer Information Bulletin, 8, 41.
Desurmont, A. (2004). Natural spawning observations Bohadschia similis. SPC Beche-de-mer Information Bulletin, 20, 37.
Dissanayake, D. C. T., & Stefanssong, G. (2010). Reproductive biology of the commercial sea cucumber Holothuria atra (Holothuroidea: Aspidochirotida) in the northwestern coastal waters of Sri Lanka. Invertebrate Reproduction Development, 54, 65-76.
Drumm, D. J., & Loneragan, N. R. (2004). Reproductive biology of Holothuria leucospilota in the Cook Islands and the implications of traditional fishing of gonads on the population. New Zealand Journal of Marine and Freshwater Research, 39(1), 141-156.
Engstrom, N. (1980). Reproductive cycles of Holothuria (Halodeima) floridana, H. (H.) mexicana and their hybrids (Echinodermata: Holothuroidea) in southern Florida, USA. International Journal Invertebrate Reproduction, 2, 237-244.
Fenberg, P. B., & Roy, K. (2008). Ecological and evolutionary consequences of size-selective harvesting: How much do we know? Molecular Ecology, 17, 209-220.
Foglietta, L. M., Camejo, M. I., Gallardo, L., & Herrera, F. C. (2004). A maturity index for holothurians exhibiting asynchronous development of gonad tubules. Journal of Experimental Marine Biology and Ecology, 303, 19-30.
Foley, J., Alvarez, M., Moore, R., Requena, E., & Warns, D. (2015). Ridge to reef water quality. Port Honduras Marine Reserve, Monkey River, Rio Grande. Marine and freshwater water quality monitoring annual report. Punta Gorda Town: Toledo Institute for Development and Environment.
Fuente-Betancourt, M. G., Jesús-Navarrete, A., Sosa-Cordero, E., & Herrero-Perezrul, M. D. (2001). Assessment of the sea cucumber (Echinodermata : Holothuroidea) as potential fishery resource in Banco Chincorro, Quintana Roo, Mexico. Bulletin of Marine Science, 68(1), 59-67.
Galigher, A. E., & Kozloff, E. N. (1971). Essentials of Practical Microtechniques (2° ed). Philadelphia: Lea and Febiger.
Ghiselin, M. T. (1969). The evolution of hermaphroditism among animals. Quarterly Review of Biology, 44, 189-208.
Global Companies. (2015). Haitian sea products. Retrieved from http://www.companiess.com/haitian_sea_products_info1332128.html
Guzman, H. M., & Guevara, C. A. (2002). Population structure, distribution and abundance of three commercial species of sea cucumber (Echinodermata) in Panama. Caribbean Journal of Science, 38(3-4), 230-238.
Guzman, H. M., Guevara, C. A., & Hernandez, I. C. (2003). Reproductive cycle of two commercial species of sea cucumber (Echinodermata: Holothuroidea) from Caribbean Panama. Marine Biology, 142(2), 271-279.
Hamel, J. F, Himmelman, J. H., & Dufresne, L. (1993). Gametogenesis and spawning of the sea cucumber Psolus fabricii (Duben and Koren). Biological Bulletin, 184, 125-143.
Hamel, J. F., & Mercier, A. (1995). Spawning of the sea cucumber Cucumaria frondosa in the St Lawrence Estuary, eastern Canada. SPC Beche-de-Mer Information Bulletin, 7, 12-18.
Hamel, J. F. & Mercier, A. (1996). Evidence of chemical communication during the gametogenesis of holothuroids. Ecology, 77, 1600-1616.
Hasbún, C. R., & Lawrence, A. J. (2002). An annotated description of shallow water Holothurians (Echinodermata: Holothuroidea) from Cayos Cochinos, Honduras. Revista de Biología Tropical, 50(2), 669-678.
Hemminga, M. A., Slim, F. J., Kazungu, J., Gansen, G. M., Nieywenhuize, J., & Kruyt, N. M. (1994). Carbon outwelling from a mangrove forest with adjacent seagrass beds and coral reefs (Gazi Bay, Kenya). Marine Ecology Progress Series, 106, 291-301.
Hendler, G., Miller, J. E., Pawson, D., & Kier, P. M. (1995). Sea stars, sea urchins and allies: echinoderms of Florida and the Caribbean. Washington: Smithsonian Institution Press.
Hendler, G., & Pawson, D. L. (2000). Echinoderms of the rhomboidal cays, Belize: biodiversity, distribution and ecology. Atoll Research Bulletin, 479, 273-299.
Herrero-Pérezrul, M. D., Reyes-Bonilla, H., & García-Domínguez, F. (1998). Casual hermaphroditism in gonochoric Isostichopus fuscus (Ludwig, 1875) (Echinodermata: Holothuroidea) of the Southern Gulf of California, Mexico. Bulletin of Marine Science, 3(63), 611-615.
Herrero-Perezrul, M. D., Reyes Bonilla, H., Garcia-Dominguez, F., & Cintra-Buenrostro, C. E. (1999). Reproduction and growth of Isostichopus fuscus (Echinodermata: Holothuroidea) in the southern Gulf of California, Mexico. Marine Biology, 135, 521-532.
Hopper, D. R., Hunter, C. L., & Richmond, R. H. (1998). Sexual reproduction of the tropical sea cucumber, Actinopyga mauritana (Echinodermata: Holothuroidea), in Guam. Bulletin of Marine Science, 63(1), 1-9.
IBM Corp. (2012). IBM SPSS Statistics for Windows (Version 21.0). Armonk, NY: IBM Corp.
Jamaica Observer. (2015). Gov’t bans sea cucumber fishing ahead of J$30-m study. Retrieved from http://www.jamaicaobserver.com/news/Gov-t-bans-sea-cucumber-fishing-ahead-of-J-30-m-study
Kong, A. (2016). The sea cucumber fishery in Jamaica. Retrieved from http://www.infopesca.org/sites/default/files/complemento/actividadesregionales/adjuntos/1215/5.5-Pepinodemar-Jamaica.pdf
Krishnaswamy, S., & Krishnan, S. (1967). A report on the reproductive cycle of the holothurian Holothuria scabra Jaeger. Current Science, 36, 155-156.
Leite-Castro, L. V., de Souza Junior, J., Brito Salmito-Vanderley, S. C., Ferreira Nunes, J., Hamel, J. F., & Mercier, A. (2016). Reproductive biology of the sea cucumber Holothuria grisea in Brazil: importance of social and environmental factors in breeding coordination. Marine Biology, 163(67), 1-13.
Masters, J. (2014). CRFM Statistics and Information Report - 2012. CRFM Secretariat Belize and St. Vincent and the Grenadines. Retrieved from http://www.crfm.net/images/CRFM_Statistics_and_Information_Report_2012_final_draft_27_Jan_2015_1_1.pdf
McEuen, F. S. (1988). Spawning behaviors of northeast Pacific sea cucumbers (Holothuroidea: Echinodermata). Marine Biology, 98, 565-585.
Mercier, A., Battaglene, S., & Hamel, J. F. (2000). Periodic movement, recruitment and size-related distribution of the sea cucumber Holothuria scabra in Solomon Islands. Hydrobiologia, 440, 81-100.
Mercier, A., & Hamel, J. F. (2009). Endogenous and exogenous control of gametogenesis and spawning in echinoderms. Advances on Marine Biology, 55(09), 1-302.
Mercier, A., Ycaza, R. H., & Hamel, J. F. (2007). Long-term study of gamete release in a broadcast-spawning holothurian: predictable lunar and diel periodicities. Marine Ecology Progress Series, 329, 179-189.
Mobile Geographics. (2016). Tide table: Belize City, Belize. Retrieved from http://tides.mobilegeographics.com/calendar/year/493.html?y=2015&m=1&d=1
Mosher, C. (1982). Spawning behaviour of the aspidochirote holothurian Holothuria mexicana Ludwig. In J. M. Lawrence (Ed.), Proceedings of the International Echinoderm Conference (pp. 467-468). Tampa Bay: A.A. Balkema, Rotterdam.
Muthiga, N. (2006). The reproductive biology of a new species of sea cucumber, Holothuria (Mertensiothuria) arenacava in a Kenyan marine protected area: the possible role of light and temperature on gametogenesis and spawning. Marine Biology, 149(3), 585-593.
NASA. (2015). MODIS Chlorophyll-a Concentration. Retrieved from http://oceancolor.gsfc.nasa.gov/cgi/browse.pl?sen=am
National Meteorological Service of Belize. (2016). Climate Summary. Retrieved from http://www.hydromet.gov.bz/climate-summary
National Meteorological Service of Belize. (2017). Climate Summary. Retrieved from http://www.hydromet.gov.bz/climate-summary
Navarro, P. G., García-Sanz, S., & Tuya, F. (2012). Reproductive biology of the sea cucumber Holothuria sanctori (Echinodermata: Holothuroidea). Scientia Marina, 76(4), 741-752.
Pawson, D. L. (1976). Shallow-water sea cucumbers (Echinodermata: Holothuroidea) from Carrie Bow Cay, Belize. Proceedings of the Biological Society of Washington, 89(31), 369-382.
Perez, A., & Garcia, O. D. (2012). Socioeconomic assessment of the sea cucumber fishery in Belize. Belmopan, Belize: University of Belize Environmental Research Institute.
Pukk, L., Kuparinen, A., Järv, L., Gross, R., & Vasemägi, A. (2013). Genetic and life-history changes associated with fisheries-induced population collapse. Evolutionary Applications, 6, 749-760.
Ramdeen, R., Belhabib, D., Harper, S., & Zeller, D. (2012). Reconstruction of total marine fisheries catches for Haiti and Navassa Island (1950-2010). In S. Harper, K. Zylich, L. Boonazaier, F. Le Manach, D. Pauly, & D. Zellet (Eds.), Fisheries Catch Reconstructions: Islands, Part II (pp. 37-45). Vancouver: University of British Columbia.
Ramofafia, C., Battaglene, S. C., Bell, J. D., & Byrne, M. (2000). Reproductive biology of the commercial sea cucumber Holothuria fuscogilva in the Solomon Islands. Marine Biology, 136, 1045-1056.
Rasolofonirina, R., Vaitilingon, D., Eeckhaut, I., & Jangoux, M. (2007). Reproductive cycle of edible echinoderms from the Southwestern Indian Ocean II: The Sandfish Holothuria scabra (Jaeger, 1833). Western Indian Ocean Journal of Marine Science, 4(1), 61-75.
Reichenbach, N. (1999). Ecology and fishery biology of Holothuria fuscogilva (Echinodermata: Holothuroidea) in the Maldives, Indian Ocean. Bulletin of Marine Science, 64(1), 103-113.
Reitzel, A. M., Miner, B. G., & McEdward, L. R. (2004). Relationships between spawning date and larval development time for benthic marine invertebrates: a modeling approach. Marine Ecology Progress Series, 280, 13-23.
Roberts, C. M., & Polunin, N. V. C. (1991). Are marine reserves effective in management of reef fisheries? Reviews in Fish Biology and Fisheries, 1(1), 65-91.
Rodriguez-Milliet, E., & Pauls, S. M. (1998). Sea cucumber fisheries in Venezuela. In R. Mooi (Ed.), Proceedings of the 9th International Echinoderm Conference (pp. 513-516). San Fransisco, California, USA: Balkema, Rotterdam.
Rogers, A. (2013). Density, abundance and distribution of sea cucumbers in Belize. Proceedings of the Gulf and Caribbean Fisheries Initiative (pp. 483-486). Chorpus Christi, Texas, USA: Gulf and Caribbean Fisheries Institute.
Rogers, A., Hamel, J. F., Baker, S., & Mercier, A. (2018). The 2009-2016 Belize sea cucumber fishery: Resource use patterns, management strategies and socioeconomic impacts. Regional Studies in Marine Science, 22, 9-20.
Rogers, A., Hamel, J. F., & Mercier, A. (2017). From life-sustaining to life-threatening: The case of the sea cucumber fishery in Nicaragua. SPC Beche-de-Mer Information. Bulletin, 37, 48-50.
SAGARPA (2015). Closed seasons for marine and freshwater species. Retrieved from http://www.conapesca.gob.mx/work/sites/cona/resources/PDFContent/14619/presentaioc. pdf
Shiell, G. R., & Uthicke, S. (2006). Reproduction of the commercial sea cucumber Holothuria whitmaei [Holothuroidea: Aspidochirotida] in the Indian and Pacific Ocean regions of Australia. Marine Biology, 148(5), 973-986.
Skewes, T., Dennis, D., & Burridge, C. (2000). Survey of Holothuria scabra (sandfish) on Warrior Reef, Torres Strait. Report to Queensland Fisheries Management Authority, Queensland, Australia. Queensland, Australia: CSIRO Division of Marine Research.
Sloan N. A., & von Bodungen, B. (1980). Distribution and feeding of the sea cucumber Isostichopus badionotus in relation to shelter and sediment criteria of the Bermuda platform. Marine Ecology Progress Series, 2, 257-264.
Smiley, S., McEuen, F., Chaffee, C., & Krishan, S. (1991). Echinodermata: Holothuroidea. In A. Giese, J. Pearse, & V. Pearse (Eds.), Reproduction of Marine Invertebrates: Echinodermata and Lophophorate (pp. 663-750). Pacific Grove, California: The Boxwood Press.
Tagliafico, A., Rangel, M. S., & Rago, N. (2011). Density and Distribution of two species of holoturoids in Cubagua Island, Venezuela. Revista de Biología Tropical, 59(2), 843-852.
Time and Date AS. (2015). Belize City, Belize - Sunrise, Sunset and Daylength. Retrieved from https://www.timeanddate.com/sun/belize/belize-city?month=1&year=2014
Toral-Granda, V. (2008). Population status, fisheries and trade of sea cucumbers in Latin America and the Caribbean. In V. Toral-Granda, A. Lovatelli, & M. Vasconcellos (Eds.), Sea Cucumbers: A Global Review of Fisheries and Trade (pp. 211-229). FAO Fisheries and Aquaculture Technical Paper No. 516. Rome: FAO.
Toral-Granda, M. V., Alvarado, J. J., Benavides, M., Ortiz, P., Mercier, A., & Hamel, J. F. (2013). Holothuria mexicana. Retrieved from http://www.iucnredlist.org/details/180492/0
Toral-Granda, M. V., & Martínez, P. C. (2007). Reproductive biology and population structure of the sea cucumber Isostichopus fuscus (Ludwig, 1875) (holothuroidea) in Caamaño, Galápagos Islands, Ecuador. Marine Biology, 151, 2091-2098.
UNESCO World Heritage Center. (2017). Belize barrier reef reserve system. Retrieved from http://whc.unesco.org/en/list/764
Unsworth, R. K. F., De Leon, P. S., Garrard, S., Jompa, J., Smith, D. J., & Bell, J. J. (2008). High connectivity of Indo-Pacific seagrass fish assemblages with mangrove and coral reef habitats. Marine Ecology Progress Series, 353, 213-224.
Uthicke, S., & Benzie, J. A. H. (2000). Effect of beche-de-mer fishing on densities and size structure of Holothuria nobilis (Echinodermata: Holothuroidea) populations on the Great Barrier Reef. Coral Reefs, 19, 271-276.
Vainikka, A., & Hyvärinen, P. (2012). Ecologically and evolutionarily sustainable fishing of the pikeperch Sander lucioperca: Lake Oulujärvi as an example. Fisheries Research, 113, 8-20.
van Veghel, M. L. J. (1993). Multiple species spawning on Curacao reefs. Bulletin of Marine Science, 52, 1017-1021.
Yingst, J. (1974). The utilization of organic detritus and associated microorganisms by Parastichopus parvimensis, a benthic deposit-feeding holothurian (Doctoral dissertation). University of South California, USA. Retrieved from https://elibrary.ru/item.asp?id=7139187
Yingst, J. Y. (1982). Factors influencing rates of sediment ingestion by Parastichopus parvimensis (Clark), and epibenthic deposit-feeding holothurian. Estuarine, Coastal and Shelf Science, 14, 119-134.
Comments
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright (c) 2018 Revista de Biología Tropical